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EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts

EPH/EPHRIN signaling is essential to many aspects of tissue self-organization and morphogenesis, but little is known about how EPH/EPHRIN signaling regulates cell mechanics during these processes. Here, we use a series of approaches to examine how EPH/EPHRIN signaling drives cellular self-organizati...

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Autores principales: Kindberg, Abigail A., Srivastava, Vasudha, Muncie, Jonathon M., Weaver, Valerie M., Gartner, Zev J., Bush, Jeffrey O.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8025214/
https://www.ncbi.nlm.nih.gov/pubmed/33798261
http://dx.doi.org/10.1083/jcb.202005216
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author Kindberg, Abigail A.
Srivastava, Vasudha
Muncie, Jonathon M.
Weaver, Valerie M.
Gartner, Zev J.
Bush, Jeffrey O.
author_facet Kindberg, Abigail A.
Srivastava, Vasudha
Muncie, Jonathon M.
Weaver, Valerie M.
Gartner, Zev J.
Bush, Jeffrey O.
author_sort Kindberg, Abigail A.
collection PubMed
description EPH/EPHRIN signaling is essential to many aspects of tissue self-organization and morphogenesis, but little is known about how EPH/EPHRIN signaling regulates cell mechanics during these processes. Here, we use a series of approaches to examine how EPH/EPHRIN signaling drives cellular self-organization. Contact angle measurements reveal that EPH/EPHRIN signaling decreases the stability of heterotypic cell:cell contacts through increased cortical actomyosin contractility. We find that EPH/EPHRIN-driven cell segregation depends on actomyosin contractility but occurs independently of directed cell migration and without changes in cell adhesion. Atomic force microscopy and live cell imaging of myosin localization support that EPH/EPHRIN signaling results in increased cortical tension. Interestingly, actomyosin contractility also nonautonomously drives increased EPHB2:EPHB2 homotypic contacts. Finally, we demonstrate that changes in tissue organization are driven by minimization of heterotypic contacts through actomyosin contractility in cell aggregates and by mouse genetics experiments. These data elucidate the biomechanical mechanisms driving EPH/EPHRIN-based cell segregation wherein differences in interfacial tension, regulated by actomyosin contractility, govern cellular self-organization.
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spelling pubmed-80252142021-12-07 EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts Kindberg, Abigail A. Srivastava, Vasudha Muncie, Jonathon M. Weaver, Valerie M. Gartner, Zev J. Bush, Jeffrey O. J Cell Biol Article EPH/EPHRIN signaling is essential to many aspects of tissue self-organization and morphogenesis, but little is known about how EPH/EPHRIN signaling regulates cell mechanics during these processes. Here, we use a series of approaches to examine how EPH/EPHRIN signaling drives cellular self-organization. Contact angle measurements reveal that EPH/EPHRIN signaling decreases the stability of heterotypic cell:cell contacts through increased cortical actomyosin contractility. We find that EPH/EPHRIN-driven cell segregation depends on actomyosin contractility but occurs independently of directed cell migration and without changes in cell adhesion. Atomic force microscopy and live cell imaging of myosin localization support that EPH/EPHRIN signaling results in increased cortical tension. Interestingly, actomyosin contractility also nonautonomously drives increased EPHB2:EPHB2 homotypic contacts. Finally, we demonstrate that changes in tissue organization are driven by minimization of heterotypic contacts through actomyosin contractility in cell aggregates and by mouse genetics experiments. These data elucidate the biomechanical mechanisms driving EPH/EPHRIN-based cell segregation wherein differences in interfacial tension, regulated by actomyosin contractility, govern cellular self-organization. Rockefeller University Press 2021-04-02 /pmc/articles/PMC8025214/ /pubmed/33798261 http://dx.doi.org/10.1083/jcb.202005216 Text en © 2021 Kindberg et al. http://www.rupress.org/terms/https://creativecommons.org/licenses/by-nc-sa/4.0/This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
spellingShingle Article
Kindberg, Abigail A.
Srivastava, Vasudha
Muncie, Jonathon M.
Weaver, Valerie M.
Gartner, Zev J.
Bush, Jeffrey O.
EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts
title EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts
title_full EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts
title_fullStr EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts
title_full_unstemmed EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts
title_short EPH/EPHRIN regulates cellular organization by actomyosin contractility effects on cell contacts
title_sort eph/ephrin regulates cellular organization by actomyosin contractility effects on cell contacts
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8025214/
https://www.ncbi.nlm.nih.gov/pubmed/33798261
http://dx.doi.org/10.1083/jcb.202005216
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